Neuronal correlates of local, lateral, and translaminar inhibition with reference to cortical columns

Abstract

In the neocortex, inhibition by γ-aminobutyric acidergic (GABAergic) interneurons is essential for shaping cortical maps, which represent sensory signals. For a detailed understanding of the stream of excitation evoked, for example, by a sensory stimulus, interneurons must be identified with reference to their impact on excitatory neurons located in different laminae of the same (home) and surround columns. We analyzed the axonal projection of layer 2/3 (L2/3) interneurons with reference to geometric landmarks of cortical columns by staining neurons in acute slices of rat barrel cortex (P20-P29) and a subsequent cluster analysis using morphological parameters that described the spatial distribution of axons. The cluster analysis defined 4 main axonal projection "types" referred to as 1) "local inhibitors" (including "chandelier neurons"), 2) "lateral inhibitors," 3) "translaminar L2/3-to-L4/5 inhibitors," and 4) "translaminar L2/3-to-L1 inhibitors." The putative innervation domains established by axonal projections of the 4 types of interneurons and the dendritic domains of their target excitatory neurons were 1) L2/3 of the home column, 2) L2/3 of both the home and neighboring columns, 3) L4 and L5A of the home column, and 4) L1 and L2/3 of the home column. The quantitative analysis of the axonal projection patterns of an unselected sample of 51 interneurons located in L2/3 thus defined anatomical correlates for local, lateral, and translaminar inhibition within and between cortical columns.